Rapid developmental switch in the mechanisms driving early cortical columnar networks

Dupont, Erwan; Hanganu, Ileana L.; Kilb, Werner; Hirsch, Silke; Luhmann, Heiko J.

doi:10.1515/nf-2006-0206

Cited by 39 publications

(105 citation statements)

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“…In total our data show that the beta-oscillations specifically synchronize activity within a cortical column consistent with data from the somatosensory cortex (Dupont et al, 2006;Yang et al, 2009). This effect is strongest for superficial layers, and more modest in deep layers.…”

Section: Resultssupporting

confidence: 87%

“…If the beta-oscillations arise in thalamus, cortex or the thalamocortical loop is not clear. The CSD profile of beta-oscillations is consistent with a thalamic origin (Molnár et al, 2003), but the ability of isolated cortex to produce similar oscillations (Dupont et al, 2006) suggests that intrinsic cortical dynamics also contributes. The horizontal spread of rvSATs in visual cortex is also consistent with their generation by retinal waves.…”

Section: Discussionmentioning

confidence: 77%

“…The ability of alpha and beta band oscillations to synchronize columnar activity in vivo (present paper and Yang et al, 2009) and in vitro (Dupont et al, 2006; Sun and Luhmann, 2007) has clear implications for synaptic plasticity mechanisms and circuit formation during cortical development. The firing of neighboring ganglion cells is poorly correlated by retinal bursts (Butts and Rokhsar, 2001).…”

Section: Discussionmentioning

confidence: 78%

“…Several long-duration activity patterns occurring in immature cortex suggest two different models for SATs. A cortical generator is suggested by the existence of long-duration migrating calcium waves and electrical oscillations identified in isolated cortical slices (Garaschuk et al, 2000; Dupont et al, 2006; Allene et al, 2008) and verified in vivo (Adelsberger et al, 2005; Yang et al, 2009). On the other hand, long-duration, multi-frequency ‘mega-bursts’ occurring before eye-opening in ferret visual cortex in vivo are eliminated by enucleation (Chiu and Weliky, 2001), suggesting such activity is dependent on peripheral input, in this case spontaneous retinal waves.…”

Section: Introductionmentioning

confidence: 98%

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“Slow Activity Transients” in Infant Rat Visual Cortex:A Spreading Synchronous Oscillation Patterned by Retinal Waves

Colonnese¹,

Khazipov²

2010

J. Neurosci.

116

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A primary feature of the preterm infant electroencephalogram is the presence of large infra-slow potentials containing rapid oscillations called slow activity transients (SATs). Such activity has not been described in animal models, and their generative mechanisms are unknown. Here we use direct-current and multisite extracellular, as well as whole-cell, recording in vivo to demonstrate the existence of regularly repeating SATs in the visual cortex of infant rats before eye opening. Present only in absence of anesthesia, SATs at postnatal day 10 -11 were identifiable as a separate group of long-duration (ϳ10 s) events that consisted of large (Ͼ1 mV) negative local-field potentials produced by the summation of multiple bursts of rapid oscillatory activity (15-30 Hz). SATs synchronized the vast majority of neuronal activity (87%) in the visual cortex before eye opening. Enucleation eliminated SATs, and their duration, interevent interval, and sub-burst structure matched those of phase III retinal waves recorded in vitro. Retinal waves, however, lacked rapid oscillations, suggesting that they arise centrally. Multielectrode recordings showed that SATs spread horizontally in cortex and synchronize activity at coactive locales via the rapid oscillations. SATs were clearly different from ongoing cortical activity, which was observable as a separate class of short bursts from postnatal day 9. Together, our data suggest that, in vivo, early cortical activity is primarily determined by peripheral inputs-retinal waves in visual cortex-that provide excitatory input, and by thalamocortical circuitry, which transforms this input to beta oscillations. We propose that the synchronous oscillations of SATs participate in the formation of visual circuitry.

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Section: Resultssupporting

confidence: 87%

Section: Discussionmentioning

confidence: 77%

Section: Discussionmentioning

confidence: 78%

Section: Introductionmentioning

confidence: 98%

See 2 more Smart Citations

“Slow Activity Transients” in Infant Rat Visual Cortex:A Spreading Synchronous Oscillation Patterned by Retinal Waves

Colonnese¹,

Khazipov²

2010

J. Neurosci.

116

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“…Later-born neurons will progressively split this domain into the marginal zone (MZ), CP and subplate (SP) [36,37]. We used the Tbr1 riboprobe to label early PPL and SP populations [38,39] at mid-gestation. While in controls Tbr1+ SP cells are well separated from Tbr1+ CP cells (Figure 6a), this does not occur in cKO embryos (Figure 6a').…”

Section: Resultsmentioning

confidence: 99%

Genetic interplay between the transcription factors Sp8 and Emx2 in the patterning of the forebrain

et al. 2007

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Long‐range projections from sparse populations of GABAergic neurons in murine subplate

Boon

Clarke

Kessaris

et al. 2019

J of Comparative Neurology

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The murine subplate contains some of the earliest generated populations of neurons in the cerebral cortex, which play an important role in the maturation of cortical inhibition. Here we present multiple lines of evidence, that the subplate itself is only very sparsely populated with GABAergic neurons at postnatal day (P)8. We used three different transgenic mouse lines, each of which labels a subset of GABAergic, ganglionic eminence derived neurons. Dlx5/6‐eGFP labels the most neurons in cortex (on average 11% of NEUN+ cells across all layers at P8) whereas CGE‐derived Lhx6‐Cre::Dlx1‐Venus fl cells are the sparsest (2% of NEUN+ cells across all layers at P8). There is significant variability in the layer distribution of labeled interneurons, with Dlx5/6‐eGFP and Lhx6‐Cre::R26R‐YFP being expressed most abundantly in Layer 5, whereas CGE‐derived Lhx6‐Cre::Dlx1‐Venus fl cells are least abundant in that layer. All three lines label at most 3% of NEUN+ neurons in the subplate, in contrast to L5, in which up to 30% of neurons are GFP+ in Dlx5/6‐eGFP. We assessed all three GABAergic populations for expression of the subplate neuron marker connective tissue growth factor (CTGF). CTGF labels up to two‐thirds of NEUN+ cells in the subplate, but was never found to colocalize with labeled GABAergic neurons in any of the three transgenic strains. Despite the GABAergic neuronal population in the subplate being sparse, long‐distance axonal connection tracing with carbocyanine dyes revealed that some Gad65‐GFP+ subplate cells form long‐range axonal projections to the internal capsule or callosum.

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Rapid developmental switch in the mechanisms driving early cortical columnar networks

Cited by 39 publications

References 0 publications

“Slow Activity Transients” in Infant Rat Visual Cortex:A Spreading Synchronous Oscillation Patterned by Retinal Waves

“Slow Activity Transients” in Infant Rat Visual Cortex:A Spreading Synchronous Oscillation Patterned by Retinal Waves

Genetic interplay between the transcription factors Sp8 and Emx2 in the patterning of the forebrain

Long‐range projections from sparse populations of GABAergic neurons in murine subplate

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